Origin and Evolution of the Powdery Mildews (Ascomycota, Erysiphales)

mycoscience 54 (2013) 75e86 Available online at www.sciencedirect.com ISSN 1340-3540 (print), 1618-2545 (online) journal homepage: www.elsevier.com/locate/myc Review Origin and evolution of the powdery mildews (Ascomycota, Erysiphales) Susumu Takamatsu* Department of Bioresources, Graduate School, Mie University, 1577 Kurima-Machiya, Tsu 514-8507, Japan article info abstract Article history: Molecular phylogeny suggests a close relationship of Asteraceae to the early evolution of Received 2 August 2012 Golovinomyces. The family Asteraceae, with a geographic origin in South America, expanded Accepted 15 August 2012 into the Northern Hemisphere, where it may have been infected by an ancestor of Golo- Available online 29 September 2012 vinomyces, thus starting a close hosteparasite relationship. Using this event as a calibration point, we designed molecular clocks for powdery mildews using the 28S rDNA D1/D2 and Keywords: internal transcribed spacer (ITS) regions. According to these clocks, the powdery mildews Biogeography originated in the Late Cretaceous and the first radiation of the major lineages occurred at Erysiphaceae the Cretaceous/Paleogene boundary. Ancestral powdery mildews may have first radiated Molecular clock on broad-leaved deciduous trees in the high latitudes of the Northern Hemisphere, and Molecular phylogeny continued further speciation whilst migrating to southward during the world cooling in the Paleogene Paleogene and Neogene periods. The cradle of four herb infecting genera, viz. Blumeria, Golovinomyces, Leveillula, and Neoe¨rysiphe may be within the area extending from Central/ West Asia to the Mediterranean. ª 2012 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved. 1. Introduction or Ferns (Amano 1986). Of the total host species, 9176 are dicotyledons, the remaining 662 being monocotyledons. Of Powdery mildews are an important group of plant pathogenic the monocotyledons, 634 species belong to the subfamily fungi forming a white, powdery film on leaves, stems, flowers, Pooideae of Poaceae (the grass family). and fruits of Angiosperms. Sixteen genera and ca 900 species Several scientific speculations on phylogenetic relation- are presently known worldwide (Braun and Cook 2012). All of ships and evolution of powdery mildews based on the species are exclusively obligate biotrophs of plants. morphology and host relationships have been published Molecular phylogenetic analyses so far reported indicate that (Neger 1901; Arnaud 1921; Raymond 1927; Blumer 1933; the powdery mildews form a distinct monophyletic group Katumoto 1973; Braun 1987, 1995). Most of these arguments (Mori et al., 2000a,b; Wang et al., 2006a,b). They may be simply devolved around characteristics thought to be primi- a fungal group that acquired an obligate biotrophic nature tive or derived. Some critical characteristics are as follows: only once in their ancestry and have retained it ever since. Up (1) number of asci in an ascoma, e.g. one or several; (2) number to 9838 plant species have been recorded as hosts of powdery of ascospores in an ascus, e.g. eight or fewer; (3) morphology mildews, all of which are Angiosperms but not Gymnosperms of appendages; (4) conidiogenesis, conidia maturing in chains, * Tel.: þ81 59 231 9497; fax: þ81 59 231 9540. E-mail address: [email protected]. 1340-3540/$ e see front matter ª 2012 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.myc.2012.08.004 76 mycoscience 54 (2013) 75e86 catenescent (Euoidium-type) or maturing one at a time (Pseu- 2.2. Speculation on evolutionary dating in the absence of doidium-type); (5) mycelium, ectotrophic or endotrophic. Of a molecular clock these, most scientists consistently regarded eight-spored asci and mycelioid appendages as primitive characters. These Since all members of powdery mildews are obligate biotrophs arguments were reviewed in Braun (1987, 1995) and Braun and of plants and their hosts are restricted to Angiosperms, the Cook (2012). appearance of a typical powdery mildew cannot pre-date the Hirata (1966) and Amano (1986) constructed a comprehen- Angiosperms. Also, since the monocotyledonous hosts are sive, worldwide list of powdery mildews and their host plants mostly restricted to the subfamily Pooideae of Poaceae, it is based on nearly 4000 references. It consists of 14,647 powdery likely that a dicot infecting powdery mildew spread to an mildew/host combinations, and the countries where they ancestor of Pooideae after the monocot/dicot split. From these were recorded (Amano 1986). This list has been utilized by assumptions it may be possible to speculate the earliest origin many scientists as a comprehensive database of powdery of powdery mildews. mildews and their hosts. The biogeography, phylogeny and The origin of Angiosperms based on the molecular clock is evolution of the powdery mildews were discussed with not congruent with the estimates of fossil ages. Calibration by reference to the data (Hirata 1968, 1969, 1971a,b, 1972, 1975, molecular clock suggests Angiosperms first appeared in the 1976, 1980; Amano 1986, 1992, 2002). These papers provide Early-Middle Jurassic Period [179e158 Ma] (Wikstro¨m et al. a unique insight into these subjects because other scientists 2001). On the other hand, fossil records indicate that Angio- have mostly based such arguments solely on morphology. sperms first appeared in northern Gondwana during the Early Since previous studies on molecular phylogeny of the Cretaceous Period, approximately 135 Ma (Barrett and Willis powdery mildews have already been reviewed in Braun et al. 2001). The oldest fossil of a monocot was found in the (2002), Takamatsu (2004), Glawe (2008) and Braun and Cook United States from Late Cretaceous sediments [90 Ma] (2012), this review is focused on two other aspects, viz. (Gandolfo et al. 1998). The molecular clock suggests that evolutionary dating and geographic origin of the powdery monocots have originated in Late Jurassic (Wikstro¨ m et al. mildews. 2001). Based on these reports, it is unlikely that powdery mildews originated earlier than the Jurassic Period. 2. Evolutionary dating of powdery mildews 2.3. Design of molecular clocks for powdery mildews The evolution of an organism is mostly driven by the Earth’s Mori et al. (2000b) determined the nucleotide sequences of the environmental changes and the concurrent evolution of other 18S and 28S rDNA for ten powdery mildew species and used organisms. Host plants are an absolute prerequisite for the them to determine the phylogenetic placement of powdery survival of an obligate biotroph like a powdery mildew. So we mildews in the Ascomycota. They used the molecular clocks cannot discuss the evolution of powdery mildews without of 18S rDNA reported by Simon et al. (1993) (0.667% per lineage relating them to the evolution of their hosts. Thus Earth’s per 100 Ma) and Berbee and Taylor (1993) (1.0% per lineage per environmental changes influence the evolution of powdery 100 Ma). Simon et al. (1993) used the monocot/dicot split mildews either directly or indirectly via their effects on host [200 Ma] as a calibration point. However, subsequent studies plants. Therefore, an estimation of the date of evolutionary estimate the split to have occurred later than 200 Ma events is essential to discuss the evolution of powdery (Gandolfo et al. 1998; Wikstro¨ m et al. 2001). Thus, the molec- mildews in relation to their hosts and environmental factors. ular clock of Simon et al. (1993) may be too slow. It is note- worthy that Berbee and Taylor used several fossil records as 2.1. Fossil record of powdery mildews calibration points for their molecular clock that was later changed to 1.26% per 100 Ma based on a re-assessment of Whilst fossil records are commonly used as direct evidence of fossil records (Berbee and Taylor’s 2001), and so their molec- evolution, they are relatively rare in fungi compared with ular clock may be more reliable than that of Simon et al’s. 1993 those of animals and plants and there is no reliable fossil clock. Berbee and Taylor’s 1993 molecular clock and 18S rDNA record, especially for powdery mildews (Braun and Cook sequences estimated the split of powdery mildews from 2012). According to a summary of fungal fossils by Tiffney Myxotrichaceae (putative sister group of powdery mildews) as and Barghoorn (1974), so far four records have been listed, of 127 Æ 24 Ma, and the first divergence within the powdery which the most reliable, named Protoascon missouriensis was mildews as 92 Æ 24 Ma, both of which suggest powdery discovered in the mid Pennsylvanian Epoch of the Permian mildews originated in the Cretaceous Period. Berbee and Period in strata laid down ca 300 million years ago (Ma) (Batra Taylor’s 2001 clock (1.26% per 100 Ma) resulted in the split et al. 1964). However, subsequent studies re-interpreted this and divergence dates of 101 and 73 Ma, respectively, still record as a kind of zygomycete fungus (Pirozynski 1976; Taylor suggesting a cretaceous origin of powdery mildews (Fig. 1). et al. 2005). Stubblefield and Taylor (1983) re-investigated the The maximum genetic divergence of the 18S rDNA within fossil Traquairia found in coal balls of the same epoch, and the powdery mildews was only 1.85% and the maximum reported that it is most similar to the Eurotiales or Erysiphales. substitutions were only 37 bases. This rate of change of 18S However, as far as I can see from the photo, there is no strong rDNA may be too slow to calibrate evolutionary dating within evidence to consider it a member of the Erysiphales. A powdery mildews. Furthermore, Berbee and Taylor’s 2001 comprehensive recent overview on fossil fungi was published clock did not include fossil records of powdery mildews, and by Taylor and Krings (2005). there is no evidence that their 18S rDNA evolves at the same mycoscience 54 (2013) 75e86 77 asteraceous hosts with Golovinomyces in early evolution.

Load more